Long-term electrophysiological changes in athletes with a history of multiple concussions

Primary objective: This event-related potentials study investigated the long-term effects associated with a history of one or multiple concussions on the N2pc and P3 components using a visual search oddball paradigm. Methods and procedure: A total of 47 university football players were assigned to three experimental groups based on prior concussion history: Athletes with a history of one concussion (single-concussion group); Athletes with two or more concussions (multi-concussion group); non-concussed athletic controls. The average post-concussion period was 31 months for athletes in the multi-concussion group and 59 months for the single-concussion group. Results: This study found significantly suppressed P3 amplitude in the multi-concussed athletes group compared to the single-concussion and non-concussed athletes even when using the time since the latest concussion as a covariate. Conclusion: This finding suggests that the multi-concussed athletes group showed long-lasting P3 amplitude suppression when compared with single-concussion or non-concussed athletes despite equivalent neuropsychological test scores and post-concussion symptoms self-reports. This pattern of results is important because it shows that ‘old’ concussions do not cause general or ubiquitous electrophysiological suppression. The specificity of the long-term effects of previous concussions to the P3, along with an intact N2pc response, suggests that further work may allow one to pinpoint the cognitive system that is specifically affected by multiple concussions.

[1]  S. Luck,et al.  Electrophysiological correlates of feature analysis during visual search. , 1994, Psychophysiology.

[2]  Risa Sawaki,et al.  Severity of AD/HD symptoms and efficiency of attentional resource allocation , 2006, Neuroscience Letters.

[3]  S. Luck,et al.  Bridging the Gap between Monkey Neurophysiology and Human Perception: An Ambiguity Resolution Theory of Visual Selective Attention , 1997, Cognitive Psychology.

[4]  Differences in Attentional Set Between Athletes and Nonathletes , 2004, The Journal of general psychology.

[5]  J Dvorak,et al.  Summary and agreement statement of the 2nd International Conference on Concussion in Sport, Prague 2004. , 2005, British journal of sports medicine.

[6]  Nicolas Robitaille,et al.  Attentional control and capture in the attentional blink paradigm: Evidence from human electrophysiology , 2006 .

[7]  Arthur F. Kramer,et al.  Assessing the development of automatic processing: An application of dual-task and event-related brain potential methodologies , 1988, Biological Psychology.

[8]  J. Polich,et al.  Attention, probability, and task demands as determinants of P300 latency from auditory stimuli. , 1986, Electroencephalography and clinical neurophysiology.

[9]  F Lepore,et al.  Concussions in athletes produce brain dysfunction as revealed by event‐related potentials , 2000, Neuroreport.

[10]  Stephen W Marshall,et al.  Cumulative effects associated with recurrent concussion in collegiate football players: the NCAA Concussion Study. , 2003, JAMA.

[11]  K. Weissenborn,et al.  P300 after minor head injury (a follow-up examination). , 1998, Acta neurologica Belgica.

[12]  Grant L Iverson,et al.  Cumulative Effects of Concussion in High School Athletes , 2002, Neurosurgery.

[13]  Nicolas Robitaille,et al.  On the control of visual spatial attention: evidence from human electrophysiology , 2006, Psychological research.

[14]  A Pfefferbaum,et al.  Apparent response incompatibility effects on P3 latency depend on the task. , 1986, Electroencephalography and clinical neurophysiology.

[15]  K. Sundet,et al.  ERP indicators of disturbed attention in mild closed head injury: a frontal lobe syndrome? , 1999, Psychophysiology.

[16]  Daniel M. Bernstein,et al.  Information processing difficulty long after self-reported concussion , 2002, Journal of the International Neuropsychological Society.

[17]  Douglas D. Potter,et al.  Changes in event-related potentials in a three-stimulus auditory oddball task after mild head injury , 2001, Neuropsychologia.

[18]  Geoffrey F Woodman,et al.  Serial deployment of attention during visual search. , 2003, Journal of experimental psychology. Human perception and performance.

[19]  H. Nordby,et al.  Information processing deficits in head injury assessed with ERPs reflecting early and late processing stages , 2000, Neuropsychologia.

[20]  Centersfordiseasecontrolandpr.  Sports-related recurrent brain injuries--United States. , 1997, MMWR. Morbidity and mortality weekly report.

[21]  B. Giordani,et al.  Disability caused by minor head injury. , 1981, Neurosurgery.

[22]  Lippincott Williams Wilkins,et al.  Practice Parameter , 1997, Neurology.

[23]  Benoit Brisson,et al.  Electrophysiological evidence of central interference in the control of visuospatial attention , 2007, Psychonomic bulletin & review.

[24]  Jeff Miller,et al.  Jackknife-based method for measuring LRP onset latency differences. , 1998, Psychophysiology.

[25]  M. R. Ford,et al.  Evoked Potential Findings in Mild Traumatic Brain Injury 1: Middle Latency Component Augmentation and Cognitive Component Attenuation , 1996 .

[26]  I. Reinvang.  Cognitive Event-Related Potentials in Neuropsychological Assessment , 1999, Neuropsychology Review.

[27]  E. Donchin,et al.  A multivariate approach to the analysis of average evoked potentials. , 1966, IEEE transactions on bio-medical engineering.

[28]  A. Starr,et al.  P300 latency correlates with digit span. , 1983, Psychophysiology.

[29]  A. Holbourn.  MECHANICS OF HEAD INJURIES , 1943 .

[30]  E Donchin,et al.  A metric for thought: a comparison of P300 latency and reaction time. , 1981, Science.

[31]  J. Polich.  P300 clinical utility and control of variability. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[32]  Fred L. Steinberg,et al.  A prospective functional MR imaging study of mild traumatic brain injury in college football players. , 2004, AJNR. American journal of neuroradiology.

[33]  J. Polich.  Clinical application of the P300 event-related brain potential. , 2004, Physical medicine and rehabilitation clinics of North America.

[34]  M. Gaetz,et al.  Electrophysiological evidence for the cumulative effects of concussion. , 2000, Brain injury.

[35]  M. Eimer.  The N2pc component as an indicator of attentional selectivity. , 1996, Electroencephalography and clinical neurophysiology.

[36]  E Donchin,et al.  Effects of mnemonic strategy manipulation in a Von Restorff paradigm. , 1990, Electroencephalography and clinical neurophysiology.

[37]  M Gaetz,et al.  The Current Status of Electrophysiologic Procedures for the Assessment of Mild Traumatic Brain Injury , 2001, The Journal of head trauma rehabilitation.

[38]  R Dell'Acqua,et al.  Spatial attention freezes during the attention blink. , 2006, Psychophysiology.

[39]  R. Werner,et al.  Multimodality evoked potential testing in acute mild closed head injury. , 1991, Archives of physical medicine and rehabilitation.

[40]  Michael McCrea,et al.  Immediate Neurocognitive Effects of Concussion , 2002, Neurosurgery.

[41]  A. Moritz,et al.  MECHANISMS OF HEAD INJURY. , 1943, Annals of surgery.

[42]  M. Lovell,et al.  Does loss of consciousness predict neuropsychological decrements after concussion? , 1999, Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine.

[43]  E. Donchin,et al.  On quantifying surprise: the variation of event-related potentials with subjective probability. , 1977, Psychophysiology.

[44]  R. Sangal,et al.  Closed head injury patients with mild cognitive complaints without neurological or psychiatric findings have abnormal visual P300 latencies , 1996, Biological Psychiatry.

[45]  J. Polich,et al.  Visual P3a in male alcoholics and controls. , 1999, Alcoholism, clinical and experimental research.

[46]  Andrew J. Saykin,et al.  Differential Working Memory Load Effects after Mild Traumatic Brain Injury , 2001, NeuroImage.

[47]  E Donchin,et al.  On how P300 amplitude varies with the utility of the eliciting stimuli. , 1978, Electroencephalography and clinical neurophysiology.

[48]  M. Lassonde,et al.  Visual P300 Effects Beyond Symptoms in Concussed College Athletes , 2004, Journal of clinical and experimental neuropsychology.

[49]  J. Hooymans,et al.  WORSENING OF DIABETIC RETINOPATHY WITH STRICT CONTROL OF BLOOD SUGAR , 1982, The Lancet.

[50]  E. Donchin,et al.  Is the P300 component a manifestation of context updating? , 1988, Behavioral and Brain Sciences.

[51]  E. Zemper,et al.  Two-Year Prospective Study of Relative Risk of a Second Cerebral Concussion , 2003, American journal of physical medicine & rehabilitation.

[52]  R. Emmerson,et al.  P3 latency and symbol digit performance correlations in aging. , 1989, Experimental aging research.

[53]  J. Polich.  On the clinical application of P300 , 1992, Biological Psychiatry.

[54]  S. Dikmen,et al.  Neuropsychological and psychosocial consequences of minor head injury. , 1986, Journal of neurology, neurosurgery, and psychiatry.

[55]  T W Picton,et al.  The P300 Wave of the Human Event‐Related Potential , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[56]  David C Viano,et al.  Concussion in Professional Football: Neuropsychological Testing—Part 6 , 2004, Neurosurgery.

[57]  John Polich,et al.  P300 and response time from a manual Stroop task , 1999, Clinical Neurophysiology.

[58]  Pierre Jolicoeur,et al.  A psychological refractory period in access to visual short-term memory and the deployment of visual-spatial attention: multitasking processing deficits revealed by event-related potentials. , 2007, Psychophysiology.

[59]  I. Reinvang,et al.  ERP Indices of Resource Allocation Difficulties in Mild Head Injury , 2000, Journal of clinical and experimental neuropsychology.

[60]  J. Powell,et al.  Cerebral Concussion in Athletes: Evaluation and Neuropsychological Testing , 2000, Neurosurgery.

[61]  S J Luck,et al.  Spatial filtering during visual search: evidence from human electrophysiology. , 1994, Journal of experimental psychology. Human perception and performance.

[62]  J. Polich,et al.  Bifurcated P300 Peaks: P3a and P3b Revisited? , 1988, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[63]  E. Donchin,et al.  The relation of P300 latency to reaction time as a function of expectancy. , 1980, Progress in brain research.

[64]  G. McCarthy,et al.  Augmenting mental chronometry: the P300 as a measure of stimulus evaluation time. , 1977, Science.

[65]  R. Johnson,et al.  On the neural generators of the P300: evidence from temporal lobectomy patients. , 1995, Electroencephalography and clinical neurophysiology. Supplement.

[66]  J. Polich.  P300 from a passive auditory paradigm. , 1989, Electroencephalography and clinical neurophysiology.

[67]  J. Enns,et al.  Visual Orienting in College Athletes: Explorations of Athlete Type and Gender , 2002, Research quarterly for exercise and sport.

[68]  N. Gosselin,et al.  Neurophysiological Anomalies in Symptomatic and Asymptomatic Concussed Athletes , 2006, Neurosurgery.

[69]  E. Donchin,et al.  Performance of concurrent tasks: a psychophysiological analysis of the reciprocity of information-processing resources. , 1983, Science.

[70]  L. Shutter,et al.  Prognostic Role of Proton Magnetic Resonance Spectroscopy in Acute Traumatic Brain Injury , 2006, The Journal of head trauma rehabilitation.

[71]  C. C. Duncan-Johnson.  Young Psychophysiologist Award address, 1980. P300 latency: a new metric of information processing. , 1981, Psychophysiology.

[72]  J. Kelly,et al.  Traumatic brain injury and concussion in sports. , 1999, JAMA.

[73]  R. Agosti,et al.  INTERNATIONAL SYMPOSIUM ON CONCUSSION IN SPORT , 2001 .